In our main line of research, we attempt to reunite the fields of sexual selection and social knowledge by documenting the limits of social knowledge and the use of sexually selected signals in geladas. We are focusing on three types of information that may be relevant for sexual selection in geladas. First, we hypothesize that, when assessing potential mates or competitors, geladas attend to individual attributes that were learned from previous encounters with particular individuals. It is well-known that individual recognition (i.e. when one individual recognizes another according to its distinctive characteristics) guides many decisions for primates, including decisions related to sexual selection. Second, we hypothesize that, in making reproductive decisions, geladas attend to the strength of relationships between other males and females. Surprisingly, very little research has examined how social knowledge (in this case, third party knowledge of another male’s relationship with a female) might facilitate reproductive decisions. In sum, our research focuses on three questions: (1) What are the limits of individual recognition in gelada society? 2) Among the animals geladas recognize, do they monitor male-female relationships? And, if so, do they base reproductive decisions on this information? (3) Do geladas rely on shorthand quality signals for assessment (see Sexual Selection and Signaling, below)? And, if so, do these signals substitute for or augment individual recognition?

We have been accumulating data on a population of geladas in the Simien Mountains National Park (SMNP) of Ethiopia. Geladas have several remarkable features that make them ideal for this research. First, geladas live in extremely large groups, where it is unlikely that individuals “know” (i.e. recognize) all other group members. This stands in sharp contrast to the typical small, stable primate group in which individuals recognize every other group member and repeatedly interact with the same individuals. As a result, most primates - but perhaps not geladas - have a wealth of social knowledge on the individuals around them and can use previous interactions to assess individuals and modify responses. To test this hypothesis, we have documented the limits of individual recognition using playback experiments. In fact, males actually have very little recognition of other males in their band – even males they encounter nearly every day (Bergman, 2010).

Second, in gelada society males may benefit from eavesdropping on the relationships among other males and females – mainly because female choice plays an important role in the outcome of male-male competition. We propose that males who selectively challenge rivals with weak attachments to their females should have more success at acquiring those females. To test this hypothesis, we used playback experiments to determine whether a subject male knows which males and females are associated using playback experiments. Such knowledge is necessary (but not sufficient) if males are monitoring the quality of the relationship between males and females. In a subsequent step, we are examining whether males that have weak relationships with females are selectively targeted by rival males.

Gelada Conservation

The gelada is a charismatic mammal that not only brings much-needed tourism to the area but also, as an Ethiopian endemic genus, represents a national treasure. Monitoring this species should be an important component to any wildlife management plan for the SMNP. As human populations in the area grow, the conflicts between humans and wildlife such as geladas are sure to grow as well. The SMNP receives international attention as a World Heritage Site due to its biodiversity, its high number of endemic species, and its outstanding physical features. However, this international attention is being threatened by the spread of farming and grazing in the area. The extensive impact of humans and their livestock on this afroalpine ecosystem needs to be reduced to preserve the SMNP as a sanctuary for endemics like geladas. While geladas appear to be able to compete in the face of extensive competition, this is less true for other endemics such as the Walia ibex and the Ethiopian wolf. In the long run, preserving this relatively small area for wildlife and subsequent tourism will reap benefits that far outweigh the economic value of the crops and livestock that are utilizing this area.

Since 1996, the SMNP has been on the list of World Heritage in Danger and faces severe encroachment from humans. Our research presence in the SMNP has, and will continue to, assist conservation efforts in the area. For example, in a collaborative effort with Mr. Berhanu Gebre (of the Ethiopian Parks Development and Protection Authority), we conducted a census of geladas living in and around the SMNP. Although the SMNP is the only place where geladas are officially protected, no comprehensive census of geladas in the area had ever been conducted. We submitted the results of our 2006 census for publication in the Ethiopian Journal of Science, SINET – making this data readily available to Ethiopian government officials (Beehner et al., 2007). A total of 4264 geladas were counted in the entire area. From these results, we estimate that approximately 2460 geladas were counted within the current boundary of the SMNP. This census will provide an important benchmark for future gelada population monitoring. However, the results of the current census suggest that the actual size of this gelada population is significantly lower than expected based on previous unpublished reports. We hope to conduct a similar census in 2011 to determine whether gelada numbers are increasing, remaining the same, or decreasing. As our long-term project progresses, we will continue to dedicate a fraction of our field time to park conservation efforts.

Sexual Selection and Signaling

In gelada society, males are constantly competing for their own harem of females. To avoid costly fights, they may use vocal and visual signals to assess the strength of their rivals. We hypothesize that geladas attend to signals that honestly advertise an individual’s quality or fighting ability. Although studied in other taxa, only very recently have quality signals been studied in primates. We propose that, as group size increases and the opportunity to obtain and retain information about every other group member is reduced, quality signals should become increasingly important. Thus, the unusually large groups found in gelada society may have favored the evolution of signals because individuals need to rapidly assess others based solely on external cues and not just prior experience.

Perhaps because of their unusual social organization, gelada males have conspicuous traits that are good candidates for signals of fighting ability or quality. We are focusing on two of these candidates: a red patch of skin on the chest and neck, and a highly ritualized loud call used in male displays. We hypothesize that one or both of these traits are sexually selected signals that are used to assess future rivals or mates. Testing this hypothesis involves answering 3 questions: (1) Do these traits vary with status among males? (2) Do other geladas attend to these traits when assessing potential rivals or mates? (3) If so, are there costs associated with these signals to ensure that they remain “honest” indicators of quality? Thus far, our data suggest that male chest patches do vary with status, such that redder males are associated with greater reproductive opportunities (Bergman et al., 2009). We also have preliminary data to suggest that red chest patches are associated with at least two “costs” – high testosterone and high heat loss. We are conducting similar studies with respect to the male gelada loud call, which appears to be linked to male status and quality.

Communication and the Socioecological Environment

We are also investigating other sources of selection on geladas’ vocal communication. Geladas have a rich and extensive vocal repertoire, and have unusually high-pitched vocalizations compared to primates of a similar size. We are using a variety of methods to examine the links between geladas’ multi-leveled social structure, relatively simple ecological environment, and their complex vocal repertoire. We are currently examining results from a sound transmission experiment that we have conducted in Awash National Park (Ethiopia) and the SMNP. These experiments were designed to test the Acoustic Adaptation Hypothesis, which proposes that a species’ vocalizations have acoustic features that allows for optimal transmission within that species’ native habitat. In addition to testing the influence of the physical environment on gelada vocalizations, we are collaborating with other researchers to put gelada vocalizations in phylogenetic context.

We are conducting detailed acoustic analyses to tease apart the influence of the social and ecological environment on geladas’ vocal repertoire. Using a library of chacma baboon and gelada vocalizations (collected by Thore Bergman and Aliza le Roux), we are contrasting two theories that link vocal repertoire complexity to (a) the social environment, versus (b) the ecological environment. Based on the social complexity hypothesis, we predict that gelada males, playing more social roles than chacma males, will have a larger vocal repertoire than chacmas. Novel vocalizations that evolved in the gelada lineage should be calls used during social interactions, such as variations on contact grunts. However, if the ecological environment has had a stronger selective pressure than the social environment, we would expect to find more complex vocalizations in chacma baboons’ repertoire. These calls should be linked to non-social aspects of their environment, such as predators and food discovery. In this comparison we are identifying homologous and unique vocalizations in each species’ repertoire. Because they are sister genera, unique calls likely represent new evolutionary events, allowing us to address the origins of new calls.

Male Reproductive Strategies

Among highly social animals like primates, males must navigate a complex social landscape of shifting relationships. Males may build temporary coalitions or long-lasting bonds to meet these ends. While strong male-male bonds are common in male-philopatric primates such as chimpanzee, evidence for strong male bonds in female-philopatric species is rare. Geladas provide an ideal opportunity to study how male bonds may influence male reproductive trajectories in a female-bonded species. Prior to acquiring reproductive access to females, bachelors live in cohesive all-male groups (AMG). Eventually, males ‘graduate’ from these AMGs to gain sole reproductive access to a group of females (one-male unit, or OMU). Bachelors acquire OMUs using one of several strategies: (1) challenging and defeating a current leader male, (2) submissively attaching themselves to an OMU and paring young females from the unit to form an incipient unit, or (3) capitalizing on the unstable period following a recent unit takeover to ‘size up’ the leader for a possible takeover. For a young bachelor, pursuing any of these strategies has long-term reproductive consequences. Although these strategies were described over three decades ago, we do not know why bachelors employ one strategy over another. Additionally, bachelors within the same AMG have been observed to ‘cooperate’ in attempts to overthrow leader males – yet only one male eventually reaps the reproductive benefits. We hypothesize that social bonds combined with other behavioral and hormonal factors play a role in the reproductive decisions of bachelor geladas.

In one line of our research, we are investigating the behavioral and hormonal factors that shape the reproductive trajectory of males as they move from a non-reproductive bachelor to a reproductive leader of an OMU. There are three main objectives to this research: (1) to describe interactions among bachelors within an all-male group; (2) to determine whether intra-bachelor relationships predict differential participation in agonistic encounters with reproductive males, and (3) to determine whether the ‘quality’ of a bachelor male predicts his reproductive strategy for acquiring females. We use behavioral data together with fecal hormone sampling to address these objectives in our study population of geladas. The proposed research is among the first to examine the relationship between male social bonds and reproductive trajectories in a female-philopatric species. Moreover, we are interested in exploring the conditions that allow bachelor geladas to maintain a cohesive group in light of competing self-interests.

Female Reproductive Strategies

In primate societies, male reproductive tenure can be short. While high turnover among males certainly affects male reproduction, it can affect female reproduction as well. In species that have a high rate of male “takeovers” (i.e. a change in the leader or dominant male), infanticide is a common male strategy that is hypothesized to benefit the male by bringing females with dependent offspring into estrus quickly. Males that produce offspring earlier in their tenure not only have a higher reproductive rate, but their infants are more likely to be weaned prior to another takeover. Anecdotal evidence on wild geladas suggests that infanticide following a male takeover may be a real threat for females with dependent offspring. In response to this threat, some pregnant females may spontaneously abort or produce “pseudo-sexual swellings” to mimic the signs of fertility. Indeed, such reproductive tactics have been reported in other primate species as a possible way to conserve or protect costly reproductive effort. However, the physiological mechanisms behind such reproductive strategies have never been explored in primates. Furthermore, documenting a real “conflict” between the sexes is difficult in long-lived animals with long life histories. Instances of conflict – in this case infanticide – may be opportunistic and rare. Geladas provide a unique system for studying infanticide because they have a high rate of takeovers that allows for sufficient data collection in a short amount of time. Additionally, by taking a physiological approach, it is possible to document each female’s stress response to a male takeover (with the potential for infanticide), even when it does not actually result in infanticide. Thus, the mechanisms (i.e. hormones) that underlie observed behavioral responses can yield a richer understanding of an adaptive framework (i.e. intersexual conflict). In a second line of our research, we are investigating the function and underlying physiology of female gelada reproductive strategies following male takeovers to evaluate to what degree intersexual conflict has shaped female gelada behavior.

Our main question is the following: does intersexual conflict exist in geladas? The first objective of this line of research is to describe the normative patterns of gelada reproduction in terms of gonadal hormones, sexual swellings, and female reproductive behavior. The second objective is to investigate the functional significance behind the physiology, sexual swellings, and reproductive behavior of female geladas following male takeovers. In other words, we will determine whether infanticide is a threat to female geladas and whether females have developed counterstrategies as a result.

Hormone Methods and Validation

In all our research, we utilize non-invasive methods of hormone collection from known individuals. Sophisticated methods have been developed for measuring steroid hormones from “excreta” – mainly, urine and feces. Particularly for studies of wild animals (where habituation or training to blood draws is not a feasible option), it is optimal to have non-invasive alternatives for measuring hormones. In many cases, such samples can be collected easily and without disturbing an animal, thereby allowing frequent sampling over long time periods. Moreover, because fecal sampling has been shown to smooth short-term fluctuations and diurnal variation, fecal measures can actually improve the ability to distinguish between normal pulsatile changes and genuine physiological responses to external events. However, only rarely do these methods directly measure the hormone in question. Usually the hormone of interest is virtually absent in feces, and methods that measure fecal steroids are actually measuring one to several downstream products of hormone metabolism. Consequently, any method of extracting steroid hormones from “excreta” must be properly validated both analytically and physiologically prior to measuring hormone metabolites in new species.

Much of our research has focused on validating the hormone extraction methods we use, while also trying to improve them. For her Ph.D. research, Jacinta Beehner modified a method of fecal steroid extraction for use in the field, where access to a freezer is limited (Beehner & Whitten, 2004). She validated this method both analytically and physiologically for use in three species of baboons and geladas (Beehner & McCann, 2008, Beehner et al., 2009). Furthermore, we have tried to improve upon this method at each stage. For example, we were able to determine that (1) diurnal rhythms do not affect fecal hormones for any of these species, (2) vortexing fecal samples in organic solvent increases hormone recovery, (3) hormones can be stored at ambient temperature for up to 4 weeks prior to freezing, and (4) freeze/thaw cycles should be limited to 1-2 cycles only or hormones are compromised (Beehner & Whitten, 2004; Pappano et al., 2010).

Genetics in a Multi-Level Society

Group living confers a variety of benefits to individuals within the group, including predator detection and defense and high rates of food acquisition. Animals that form groups with close genetic relatives may also benefit from opportunities to help kin at minimal cost, thus increasing the helper’s indirect fitness. Additionally, individuals in kin groups gain direct fitness advantages through decreased within group aggression, lowered risk of infanticide, and coalitionary support. However, much of what we know about the effects of kinship comes from relatively simple, single level social systems. We know very little about how kinship works in complex, multi-level societies like those found in modern humans. Moreover, until recently only long-term studies have had the pedigree data to map maternal relatives. Now, molecular genetic techniques that combine non-invasive sampling with PCR-based genotyping allow researchers to evaluate the interaction between relatedness and social systems in species where longitudinal data are lacking.

We apply these new genetic techniques, together with detailed behavioral sampling, to the unusual, highly complex social system of the gelada. Their social structure appears to be considerably more complex than that of their close phylogenetic relatives, the well-studied baboons. Therefore this research will provide important new data on kinship-behavior interactions and the evolution of complex societies in mammals. The goal if this research is to understand the patterns of relatedness in gelada’s multi-level society and how relatedness influences social interactions.